janssens+ritz+asthma+triggers+cande+allergy
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asthma triggersTRANSCRIPT
DOI: 10.1111/cea.12138
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Perceived Triggers of Asthma: Key to Symptom Perception and Management
Thomas Janssens1,2
& Thomas Ritz2
1 University of Leuven, Leuven, Belgium
2 Southern Methodist University, Dallas, TX, USA
Abstract
Adequate asthma management depends on an accurate identification of asthma triggers. A
review of the literature on trigger perception in asthma shows that individuals vary in their
perception of asthma triggers and that the correlation between self-reported asthma triggers
and allergy tests is only modest. In this paper, we provide an overview of psychological
mechanisms involved in the process of asthma triggers identification. We identify sources of
errors in trigger identification and targets for behavioral interventions that aim to improve the
accuracy of asthma trigger identification and thereby enhance asthma control.
The final version of this manuscript can be accessed at
http://onlinelibrary.wiley.com/doi/10.1111/cea.12138/abstract
DOI: 10.1111/cea.12138
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Introduction
Asthma and allergies are a major source of health problems. In Western and Westernized
countries, prevalence of physician diagnosed asthma is about 9-12% [1-3], while 28% report
at least 1 type of diagnosed allergic disorder (e.g, asthma, food allergy, rhinitis, dermatitis [2].
Allergic asthma and allergies have in common that symptoms occur in response to an allergic
trigger (e.g. house dust mite, pollen). In asthma, non-allergic triggers such as air pollution,
cigarette smoke, perfume, stress, negative emotions or physical activity may also trigger
asthma symptoms [4]. Management of asthma and allergies consists of pharmacological
management, combined with avoidance of triggers that cause symptom exacerbations [4, 5].
However, trigger avoidance interventions have shown mixed results, and systematic
evaluations of interventions that focus on a specific environmental control measure for a
specific trigger have shown only limited overall effects on symptoms and disease severity [6,
7].
Although it may be hard to generalize findings from the wide variety of trigger avoidance
interventions that have been evaluated [8], we argue that one reason for the mixed success of
trigger avoidance may be that individuals have difficulty identifying their personal triggers. In
patients with asthma, agreement between reported asthma triggers and actual tests of physical
or psychological trigger impact is only moderate [9]. Although this discrepancy could be due
to a lack of accuracy of the allergy test, this finding suggests that patients may be unaware of
all or some of their triggers, which may leave them uncertain about what the exacerbating
factors of their disease are and about which specific triggers to avoid, and could leave them
exposed to critical triggers repeatedly without protection. This way, they are presented with
recurrent aversive somatic experiences that appear unpredictable and uncontrollable [10, 11].
Alternatively, patients with asthma may attribute their respiratory symptoms to a specific
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trigger despite the absence of a relationship between the trigger and actual airway obstruction.
In other allergic conditions, such as food allergy, the discordance between perceived allergic
triggers and triggers identified by atopy tests or provocation tests is even worse [12, 13].
Misidentification of asthma triggers can lead to unnecessary avoidance of perceived triggers
and thus restrictions in daily functioning and impairments in quality of life. In asthma, a
discrepancy between the perception of symptoms and actual lung function effects of benign
daily life physical activity [14] could be associated with the long term risk of forgoing the
protective effect of exercise.
In this paper, we will review the empirical evidence on trigger perception in asthma, outline
psychological mechanisms that are involved in the identification of allergens or asthma
triggers, and identify potential sources of errors in trigger identification. We will conclude the
review with potential targets for interventions that aim to improve accurate trigger
identification and thus enhance patients’ perception of their disease activity.
Perceived Triggers of Asthma: Measurement, Structure, and Association with Asthma
Outcomes
Despite the importance of trigger perception in asthma management, only few studies have
investigated patients’ self-report of asthma triggers. These studies have been carried out in a
variety of settings and differ in methodology, making it difficult to compare their results. In
absence of a more established research base, we will try to distill some general findings from
these studies1.
1 The search for articles on trigger perception was conducted in Google Scholar, using the search term asthma
trigger perception OR identification, and by identifying papers that cited to key articles identified by our search
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The number of asthma triggers that is reported by patients in different studies varies widely,
ranging from 4-12 [15-17]. Differences in the number of triggers reported across studies may
be a function of the questions that are used to elicit personal trigger reports, with the number
of triggers being evaluated ranging from 9-32 [9, 15-17]. In order to assess asthma triggers in
a standardized form, studies have attempted to develop measures to probe patients’ trigger
perceptions. An earlier instrument, the Asthma Trigger Index, [18] was specifically developed
to evaluate emotional triggers of asthma. It consisted of a list of potential triggers and a series
of situation vignettes linked to emotional experiences.. Although the instrument was reported
to have a high test-retest reliability and good content validity, results of a psychometric
evaluation have never been published. More recently, the Asthma Trigger Inventory (ATI) [9]
has been developed to assess a broad spectrum of asthma triggers in a standardized way. It is
a 32-item questionnaire, consisting of 7 subscales measuring trigger domains of pollen
allergens, animal allergens, physical activity, air pollution/irritants, infections, and
psychological factors. All domain scales have a high internal consistency and test-retest
reliability.
Despite the variation in the assessment of self-reported asthma triggers, some general findings
can be drawn from this literature. Self-reported asthma triggers are associated with disease
severity and impact. Patients with a higher number of asthma triggers report less quality of
life [16]. Furthermore, a higher number of self-reported asthma triggers is correlated with
physician ratings of more severe asthma [9, 17, 19], more exacerbations, and a higher
frequency of oral corticosteroid use [9, 16]. Self-reported asthma triggers, are also associated
with more primary care visits and emergency room visits, as well as a higher rate of
hospitalization [9, 16]. Moreover, patients with a higher number of asthma triggers had a
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greater chance of relapse defined as urgent or unscheduled physician visits in the two weeks
after an emergency room visit [15].
Demographic variables appear to moderate asthma trigger reports. Consistently, female
patients report more asthma triggers than male asthma patients [16, 17, 19]. Higher education
levels are associated with the report of fewer asthma triggers [9, 19], although the latter
association is not always found [16]. Similarly, evidence for a relationship with race or
ethnicity of participants is still equivocal [9, 16].
Studies that have examined the association of different types of triggers with asthma and other
health outcomes found that self-report of animals as asthma triggers is related a lower age of
asthma onset [9, 16, 19]. Self-report of exercise as an asthma trigger is associated with obesity
[16, 20]. Emotional triggers (e.g. stress, intense emotions) are associated with more severe
asthma, occurrence of nighttime symptoms, and oral corticosteroid use [9, 17, 19].
Furthermore, emotional triggers are linked to a decrease in quality of life and increased
anxiety and depression [16, 19]. In general, trigger domains of allergic versus non-allergic
triggers appear to be relatively independent from each other and are associated differentially
with demographics, asthma manifestations, and outcomes [9, 19].
When comparing two studies that used the ATI to investigate asthma triggers in different
countries, Britain [9] and Germany [19], we noticed some differences in the relationship
between ATI subscales and specific demographics or disease-related variables (e.g., gender
differences in the report of air pollution and infections as asthma triggers). On the other hand,
consistent associations with a standardized asthma symptom exacerbation measure, the
Asthma Symptom Checklist [21] were observed, in that psychological asthma triggers were
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linked to hyperventilation symptoms [22]. In terms of the structure of trigger report,
remarkable consistency was uncovered with British [9] and German [19] adult asthma
patients as well as children with asthma in the United States [23]. The ATI subdomains of
trigger perception were also readily identified in an Indonesian sample of adult asthma
patients using the 32-item set of the ATI, but discrepancies appeared when the item pool was
expanded and factors associated with regional specifics, such as weather conditions and
specific aeroallergens, emerged [24]. These findings suggest both cross-cultural consistencies
and variations in the perception of asthma triggers. More inconsistencies exist in form of
culturally idiosyncratic trigger beliefs, such as exposure to cold foods in south Asian cultures,
or imbalances in hot and cold elements often endorsed in Guatemala and Mexico, which are
often tied to specific traditional remedies for asthma that are thought to alleviate these effects
[25, 26].
The variation in self-reported asthma triggers and association of different asthma triggers with
different demographic variables and disease outcome require further study. Although some of
this variation could be explained by the existence of different asthma phenotypes (e.g., an
adult-onset non-allergic phenotype vs. early onset atopic asthma, [27], other parts of this
variation may be clarified by examining the psychological processes involved in asthma
trigger identification.
Mechanisms of asthma trigger identification
Asthma trigger identification is a complex task. It requires perception of asthma symptoms,
perception of potential asthma triggers, and perception of a contingency or causal relationship
between potential asthma triggers and symptoms (cf. Figure 1). Each of these components of
trigger identification is associated with specific challenges. Furthermore, the components are
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not fully independent, as each of the components exerts an influence on the other. In pediatric
asthma, the task of trigger identification may be further complicated by potential parent-child
discordances on each of these components [28, 29].
Perception of Triggers and their Identification as Asthma-Relevant
Many potential asthma triggers, such as pollen, house dust mite, mold, small particulate
matter, or respiratory viruses, do not have a phenomenal appearance that is easy to perceive.
Therefore, presence of these triggers is often inferred from the occurrence of cues that are
associated with these triggers, such as trees in summer, dust, damp indoor spaces, diesel
smell, or the occurrence physical symptoms that are indicative of upper respiratory infections.
This difficulty reflects for example on the association between perceived allergic triggers and
allergy skin test results. The association between perceived allergens and skin prick test wheal
sizes is sometimes stronger for triggers with a clearer phenomenal presentation, such as cats
and dogs, than for less distinct triggers, such as pollen or molds [9, 30]. Similarly, the
availability of a potent trigger that is easy to perceive may explain why smokers report fewer
asthma triggers, especially allergic asthma triggers, compared to non-smokers [9, 16].
Prior knowledge and beliefs about potential asthma triggers and their occurrence may help
identify asthma triggers that are hard to perceive, whereas a lack of knowledge about potential
asthma triggers may hinder perception of triggers. Patients with greater knowledge about
asthma report a higher number of asthma triggers [16], whereas lack of information about the
role of mold or cockroaches as asthma triggers may hinder their perception as personally
relevant asthma triggers [30-32]. Furthermore, given the large inter-individual variability of
asthma triggers and allergic triggers [9, 33], knowledge and beliefs about common asthma
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triggers may both help and hinder identification of personal asthma triggers, depending on
whether or not general knowledge of asthma triggers matches personal susceptibilities.
Perception of asthma symptoms
The perception of asthma symptoms occurs when changes in somatosensory information are
detected and matched to mental models of asthma symptoms [34, 35]. In this process, several
factors have been identified that may cause a divergence between the level of
bronchoconstriction and the level of perceived asthma symptoms. For example, a person may
be unable to detect changes in respiratory resistance, and the resulting absence of asthma
symptoms increases the risk of near-fatal asthma [36] and may also hinder a person to
perceive a contingency between airway obstruction and environmental factors that triggers the
obstruction. Furthermore, concurrent affect or contextual information may also interfere with
the accurate perception of asthma symptoms [37-41]. Experimental studies have shown that
contextual information that is related to previous experience with asthma triggers can lead to
the perception of asthma symptoms in absence of the original asthma trigger [42], whereas
being in a situation that is perceived as unrelated to asthma may also reduce the perception of
asthma symptoms [43]. Also, other factors such as memory, personality, gender, and cultural
norms have been shown to influence perception and report of asthma symptoms [35, 44, 45].
Similar to perception of asthma symptoms, perception of other physical symptom, such as
symptoms linked to upper respiratory tract infections, is also correlated with personality
characteristics and may also lack accordance with objective disease criteria [46, 47].
However, information about the role of perception of upper respiratory tract infections in
asthma management is currently lacking.
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These examples show that perception of respiratory symptoms is a complex process that is
prone to inaccuracies. It is therefore unsurprising that inaccurate perception of asthma
symptoms is a widespread problem, with an estimated prevalence of 15 to 60%, depending on
the methodology that is used to assess it [35]. As accurate perception of asthma symptoms is a
prerequisite for accurate identification of asthma triggers, this may further complicate the
identification of asthma triggers.
Perception of Contingencies Between Triggers and Symptoms
Accurate identification of asthma triggers is dependent upon the accurate perception of a
contingency between the trigger and asthma symptoms. Humans and animals can be very
adept at identifying contingencies and rely on this ability to reduce uncertainty and
unpredictability in their environment [48]. In asthma and allergies, contingency perception is
used to predict and avoid onset of asthma symptoms. However, contingency perception is
often biased. Several studies have shown that perceived intensity or unpleasantness of an
event is associated with an overestimation of the contingency between this event and
preceding cues [49-51]. Because perceived unpleasantness and contingency perception are
associated, this may also explain the discrepancy between self-reported allergy symptoms
versus their diagnosis and treatment [52]. Indeed, in a survey on underdiagnosis and
undertreatment of allergic rhinitis, patients reported that they have had symptoms for quite
some time, but only started seeking diagnosis and treatment when their symptoms became
intolerable [53]. If individuals with rhinitis perceive their symptoms to be present yet of little
importance, this may not only lead to underdiagnosis and undertreatment, but may also leave
these individuals less inclined to identify and avoid triggers of their symptoms.
DOI: 10.1111/cea.12138
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Prior expectancies or beliefs can also have an influence on the perceived relationship between
a potential trigger and respiratory symptoms. In laboratory experiments, prior expectancies
have been shown to guide perceived contingencies and symptom reports, even when an
objective contingency between the potential trigger and respiratory symptoms was absent
[54]. Related research on anxiety disorders suggests that the effect of prior expectancies may
be dependent upon fear levels. Whereas individuals show an increased expectancy of a
negative event following fear-relevant (e.g. pictures of spiders) vs. fear-irrelevant (e.g.
pictures of mushrooms) pictures, only in high fearful individuals, this expectancy persists
after repeated confrontation with situations wherein presentation of these pictures is
noncontingent with the aversive outcome [55]. Fear and anxiety also promote other inaccurate
perceptions of contingencies that may be especially relevant for asthma trigger identification.
For example, individuals with panic disorder show an overgeneralized fear response when
confronted with cues that share perceptual similarity with a known fear cue [56].
Furthermore, after confrontation with a contingency between a cue A and an unpleasant
outcome, and confrontation with a contingency between a compound cue AB and an
unpleasant outcome, anxious individuals show sustained fear to element B, even though
confrontation with cue A and compound cue AB resulted in the same aversive outcome. [57].
Thus, anxious individuals do not learn that one of the elements of the compound cue AB, the
cue B, is unrelated to the aversive outcome. This observation is particularly relevant to the
perception of asthma triggers as many asthma triggers may co-occur in complex stimulus
configurations, which may lead individuals to experience asthma symptoms when confronted
with individual elements of the compound stimulus. For example, confrontation with asthma
symptoms in response to physical exercise may cause high anxious individuals to perceive co-
occurring cues, such as particular aspects of the environment in which the exercise takes
place, as an asthma trigger, even if physical exercise alone (e.g., on a treadmill) would cause
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the same amount of asthma symptoms. In low-anxious individuals, the perception of physical
exercise as a trigger would ‘block’ the perception of the exercise context as an asthma trigger.
These examples suggest that confrontation with an aversive outcome may lead to the adoption
of a “better safe than sorry” approach, especially in persons with asthma that are highly
fearful or have comorbid anxiety disorders. The prevalence of anxiety disorders is higher in
persons with asthma compared to the general population [58].
Other biases may occur in depressed individuals with asthma. Research on cognitive bias in
depression shows that depressed individuals are less prone to inflating contingencies when
there is no objective contingency between a cue and an outcome [59]. However, depressed
individuals do exhibit an underestimation of contingency, especially in situations where
control is important [60], which could lead to a reduction in the ability to detect asthma-
trigger contingencies in individuals with asthma and comorbid depression. Experimental
inductions of non-contingency or lack of control (learned helplessness) have similar effects on
subsequent contingency ratings and task performance [61], and individuals with asthma are
more susceptible to these effects (impaired problem solving after a learned helplessness
induction) compared to matched controls [62].
Beyond cognitive biases, actual bronchoconstriction due to emotional states [63] may be
present in anxiety disorders and depression, which might enhance the perception of
contingencies between psychological triggers and resulting symptoms, or contribute to
bronchoconstriction elicited by other triggers and therefore enhance their perception.
Temporal characteristics of the allergic response may further complicate the accurate
perception of trigger-symptom contingencies. Allergic reactions consist of both an acute
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(within minutes after exposure) as well as a late phase response (4-24 hours after initial
exposure)[64], which means that by the time the late response occurs it may not be easy to
determine what triggered the response originally. Indeed, a decrease in lung function during
the late phase response is perceived as less intense compared to a similar decrease in lung
function during the acute phase [65]. In contrast, the airway constriction to emotional triggers
happens while exposed to the trigger, thus providing a much better condition for perceiving
trigger-symptom contingencies [66]. Consequently, reports of psychological asthma triggers
in daily life have been linked to stronger bronchoconstriction to emotionally aversive
laboratory stimuli [9, 66, 67] Furthermore, allergic reactions to specific triggers have been
known to change during the lifetime response in later life [68]. This implies that previous
knowledge about individually relevant asthma triggers may become inaccurate when the
sensitivity to specific triggers changes.
Activation of the immune system may be involved in the perception of trigger-symptom
contingencies. Although no study has directly investigated the effects of inflammation on
contingency perception, stronger inflammatory responses to allergen provocation have been
found in periods of stress [69], which could make it easier to perceive trigger-symptom
contingencies. Furthermore, increased immune activation is also associated with attention for
and avoidance of disease-related cues [70]. Asthma patients also show a specific association
of airway inflammation and attention for asthma-specific cues, but not for general negative
cues [71]. This increased attention to environmental asthma-specific cues may help
identification of asthma triggers, but there is also a risk of biased contingency perception if
inflammation directs attention to asthma-specific cues that are present but not involved in the
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airway response. Furthermore, prior beliefs may interact with the effect of inflammation on
attention to potential triggers.
Bronchoconstriction due to trigger perception
Perception of an environmental agent as an asthma trigger or suggestion that an
pharmacological agent is an asthma trigger not only can elicit the perception of asthma
symptoms but also can lead to an increase in bronchoconstriction, as the large literature on
suggestion-induced bronchoconstriction shows [72]. Although the effect of suggestion on
bronchoconstriction and symptom perception appear to occur independently [73], both effects
can be conceptualized as feed-forward mechanisms, motivating a person to get away from this
context before more damage occurs. These feed-forward mechanisms may be involved in the
maintenance of perceived trigger-symptom contingencies, which in turn may have an impact
on asthma-related quality of life and may interfere with adequate self-management of asthma.
Furthermore, there are large individual differences in the effect of suggestions on symptom
experience and bronchoconstriction [72]. Further investigation of these individual differences
may also aide our understanding of asthma trigger perception.
Potential interventions
The effects of suggestion on bronchoconstriction and symptom perception, as well as the role
of contextual information and trigger beliefs on symptom perception, suggest that
interventions that try to modify trigger information or trigger beliefs can be used to correct
inaccurate perception of asthma symptoms [35]. Education about potential triggers (e.g.
allergens, irritants, respiratory infections) is an essential part of asthma management (GINA,
2010). Asthma education programs, which include education about asthma triggers and
environmental control measures have been shown to improve clinical outcomes
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(hospitalizations, emergency room visits, unscheduled doctor visits) and quality of life
[74],with newer programs tailoring information to patient needs [75, 76].
However, in day to day allergy care, problems may occur that can interfere with optimal
asthma trigger management. Although clinicians often inquire about potential asthma triggers
during appointments, education about triggers and environmental control measures is less
frequent [77]. In addition,, patients often have difficulty carrying out environmental control
measures, or may be hindered by the cost of some of these measures [78]. More problematic
is that about half of the environmental control measures that are carried out by patients are
unlikely to be beneficial on the basis of current guidelines [79].
A further potential problem with trigger education and inquiry is that alerting participants to
potential asthma triggers may promote unwarranted generalization of asthma triggers. Indeed,
knowledge about asthma is associated with a larger number of self-reported asthma triggers
[16] and experimental research has shown that informing participants about the danger of
environmental agents promotes learned symptom responses [80]. A thorough evaluation of
potential asthma triggers, including objective allergen tests may therefore help to identify
asthma triggers that the patient was previously unaware of and correct erroneous trigger
beliefs that erroneous symptom-trigger associations. For non-allergic triggers, monitoring of
triggers, peak expiratory flow and asthma symptoms in daily life may help to detect
previously unidentified and misidentified asthma triggers [81]. In order to improve
participation in physical exercise, it may be important to provide patients with a clear plan
that includes type of exercise and measures patients can take to reduce the occurrence of
asthma symptoms [82] .
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The improvement of asthma trigger management in routine clinical care also remains a
challenge. One descriptive study of urban pediatric clinic visits suggested that less than half of
the parents received advice about environmental triggers and control measures [83]. Based on
this and other shortcomings reported by clinicians and patients [77-79], it would be advisable
for clinicians to routinely inquire about potential triggers and tailor information about triggers
and environmental control methods to patient needs. Non-adherence to environmental control
measures may be avoided when they are easy to implement and follow up (e.g. simple steps
as part of an asthma action plan). Furthermore, clinicians would need to be mindful about
inaccurate trigger beliefs and use of ineffective trigger control methods.
One way to tailor information to patient needs is the combination of allergy skin prick tests
with trigger evaluation and education, which has been shown to result in the identification of
discrepancies between asthma trigger beliefs and allergic response, an increase in the
relationship between specific allergic sensitization and trigger-specific avoidance measures
and improvement of lung function, compared to a limited intervention control group [30].
Furthermore, patients receiving a trigger evaluation intervention who did not report animal
triggers among their top triggers at baseline, showed an increase in perceived animal-related
triggers at follow-up, suggesting that this type of asthma trigger education may be especially
beneficial for persons that were previously unaware of crucial asthma triggers [30]. However,
given the limited data that is available, more research on trigger identification interventions
and integration of these methods in routine clinical care is definitely needed.
Interventions that are aimed at increasing accuracy of trigger identification may be especially
beneficial for certain subgroups of individuals with asthma. For example, individuals that are
susceptible to respiratory infections may benefit more due to the synergistic effects of allergen
exposure and respiratory infections on asthma exacerbations [84]. Moreover, persons with
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comorbid asthma and panic disorder may benefit from interventions aimed at correcting
inaccurate asthma trigger beliefs, as these persons may fail to differentiate between triggers of
asthma symptoms and triggers of panic [85]. Information about differences between asthma
and panic symptoms has been included in a pilot trial for treatment of asthma and panic
disorder that has shown promising results [86]. Furthermore, misidentification of asthma
triggers that is associated with anxiety of fear about asthma triggers may benefit from
treatment strategies that are adapted from the treatment of anxiety and fear. In anxiety
disorders, the success of exposure therapy has shown that repeated exposure to fear-eliciting
cues during treatment is one of the most effective ways to reduce fear [87]. In a similar
fashion, we expect that a treatment that exposes patients to misidentified asthma triggers may
result in a reduction of potential anxieties that are associated with these triggers and in a
reduction of asthma symptoms that are associated with these misidentified triggers. Ideally,
such a treatment would be preceded by a thorough identification of perceived asthma triggers
using monitoring in daily life, lung function testing and allergy diagnosis, but due to practical
limitations (e.g. the availability of trigger challenge chambers) more limited interventions will
probably have a better chance at being implemented in routine clinical care.
Conclusion
Accurate identification of asthma triggers often is a prerequisite for adequate asthma
management. However, so far, research on the identification of asthma triggers has not
received sufficient attention. Problems with the perception of asthma symptoms and asthma
triggers as well as difficulties perceiving contingencies between triggers and symptoms may
hinder accurate identification of asthma triggers. Beliefs about asthma triggers can both help
and hinder the identification of trigger-symptom contingencies. Lack of knowledge about an
important asthma trigger may lead to a failure to identify this trigger as a personally relevant
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asthma trigger. Beliefs about asthma triggers can also lead to misidentification of asthma
triggers, although further research into the role of anxiety and fear in this misidentification is
needed. Finally, perceived asthma triggers can elicit the perception of asthma symptoms
and/or elicit bronchoconstriction, which may further complicate the accurate identification of
asthma triggers. The role of beliefs about asthma triggers in asthma trigger identification
makes them a key target for interventions that are aimed at improving identification of asthma
triggers. We have identified educational interventions, daily life monitoring, and exposure to
perceived asthma triggers as interventions that may change trigger beliefs, but further research
is needed to evaluate these interventions and study the ways in which they can improve
asthma control.
Acknowledgements
Dr. Janssens is supported by grant PDMK/11/062 of the KU Leuven Research Fund and a
travel grant of the Research Foundation - Flanders (FWO). Preparation of this manuscript was
partly funded by a National Institutes of Health/National Heart, Lung and Blood Institute
grant, R01 HL-089761 to Dr. Ritz.
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